Gene activation-associated long noncoding RNAs function in mouse preimplantation development

Development (Cambridge)

Volumn 142, Issue 5, 2015, Pages 910-920

  Hamazaki, Nobuhiko ^a,b   Uesaka, Masahiro ^a,b   Nakashima, Kinichi ^b   Agata, Kiyokazu ^a   Imamura, Takuya ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

DNA demethylation; Early mouse preimplantation development; Epigenetic regulation; Long noncoding RNA; Pluripotency; Zygotic gene activation

Indexed keywords

DNA; INTERLEUKIN 27; LONG UNTRANSLATED RNA; MESSENGER RNA; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR CDX2; TRANSCRIPTION FACTOR NANOG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BLASTOCYST; CELL DIFFERENTIATION; COLONY FORMATION; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; DEVELOPMENTAL GENE; DEVELOPMENTAL GENETICS; DNA METHYLATION; EMBRYO; EMBRYOID BODY; EXCISION REPAIR; FEMALE; GENE ACTIVATION; GENE EXPRESSION; GENE FUNCTION; GENE SILENCING; GENETIC ASSOCIATION; IN VITRO STUDY; LETHALITY; MARKER GENE; METAPHASE; MICROINJECTION; MOUSE; MOUSE EMBRYO; NICK END LABELING; NONHUMAN; POSITION WEIGHT MATRIX; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROMOTER REGION; PRONUCLEUS; RNA METHYLATION; RNA SEQUENCE; RNA TRANSCRIPTION; TRANSCRIPTION INITIATION SITE; UPREGULATION; ZONA PELLUCIDA; ANIMAL; CYTOLOGY; DATA MINING; GENETIC EPIGENESIS; GENETICS; MALE; METABOLISM; OOCYTE; PHYSIOLOGY; PLURIPOTENT STEM CELL; POLYMERASE CHAIN REACTION; PREGNANCY; SPERMATOZOON;

MUS;

ANIMALS; BLASTOCYST; DATA MINING; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; MALE; MICE; OOCYTES; PLURIPOTENT STEM CELLS; POLYMERASE CHAIN REACTION; PREGNANCY; RNA, LONG NONCODING; SPERMATOZOA;

EID: 84923301434     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.116996     Document Type: Article

References (49)

1. Alexander, S. P. H., Benson, H. E., Faccenda, E., Pawson, A. J., Sharman, J. L., Spedding, M., Peters, J. A. and Harmar, A. J.; CGTP Collaborators (2013). The concise guide to PHARMACOLOGY 2013/14: enzymes. Br. J. Pharmacol. 170, 1797-1867.
2. Aoki, F., Worrad, D. M. and Schultz, R. M. (1997). Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev. Biol. 181, 296-307.
3. Borgel, J., Guibert, S., Li, Y., Chiba, H., Schübeler, D., Sasaki, H., Forné, T. and Weber, M. (2010). Targets and dynamics of promoter DNA methylation during early mouse development. Nat. Genet. 42, 1093-1100.
4. Branco, M. R., Ficz, G. and Reik, W. (2012). Uncovering the role oÍf 5-hydroxymethylcytosine in the epigenome. Nat. Rev. Genet. 13, 7-13.
5. Braun, R. E. (2001). Packaging paternal chromosomes with protamine. Nat. Genet. 28, 10-12.
6. Brison, D. R. and Schultz, R. M. (1997). Apoptosis during mouse blastocyst formation: evidence for a role for survival factors including transforming growth factor alpha. Biol. Reprod. 56, 1088-1096.
7. Chambers, I., Colby, D., Robertson, M., Nichols, J., Lee, S., Tweedie, S. and Smith, A. (2003). Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113, 643-655.
8. Chu, C., Qu, K., Zhong, F. L., Artandi, S. E. and Chang, H. Y. (2011). Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol. Cell 44, 667-678.
9. Fabian, D., Koppel, J. and Maddox-Hyttel, P. (2005). Apoptotic processes during mammalian preimplantation development. Theriogenology 64, 221-231.
10. Farthing, C. R., Ficz, G., Ng, R. K., Chan, C.-F., Andrews, S., Dean, W., Hemberger, M. and Reik, W. (2008). Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes. PLoS Genet. 4, e1000116.
11. Fatica, A. and Bozzoni, I. (2014). Long non-coding RNAs: new players in cell differentiation and development. Nat. Rev. Genet. 15, 7-21.
12. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J. et al. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
13. Gupta, R. A., Shah, N., Wang, K. C., Kim, J., Horlings, H. M., Wong, D. J., Tsai, M.-C., Hung, T., Argani, P., Rinn, J. L. et al. (2010). Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464, 1071-1076.
14. Hajkova, P., Jeffries, S. J., Lee, C., Miller, N., Jackson, S. P. and Surani, M. A. (2010). Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329, 78-82.
15. Imamura, T., Neildez, T. M. A., Thenevin, C. and Paldi, A. (2004a). Essential role for poly (ADP-ribosyl)ation in mouse preimplantation development. BMC Mol. Biol. 5, 4.
16. Imamura, T., Yamamoto, S., Ohgane, J., Hattori, N., Tanaka, S. and Shiota, K. (2004b). Non-coding RNA directed DNA demethylation of Sphk1 CpG island. Biochem. Biophys. Res. Commun. 322, 593-600.
17. Imamura, T., Kerjean, A., Heams, T., Kupiec, J.-J., Thenevin, C. and Páldi, A. (2005). Dynamic CpG and non-CpG methylation of the Peg1/Mest gene in the mouse oocyte and preimplantation embryo. J. Biol. Chem. 280, 20171-20175.
18. Imamura, T., Uesaka, M. and Nakashima, K. (2014). Epigenetic setting and reprogramming for neural cell fate determination and differentiation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130511.
19. Jadrich, J. L., O’Connor, M. B. and Coucouvanis, E. (2006). The TGF beta activated kinase TAK1 regulates vascular development in vivo. Development 133, 1529-1541.
20. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R. and Salzberg, S. L. (2013). TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36.
21. Kohli, R. M. and Zhang, Y. (2013). TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502, 472-479.
22. Latham, K. E., Garrels, J. I., Chang, C. and Solter, D. (1991). Quantitative analysis of protein synthesis in mouse embryos. I. Extensive reprogramming at the oneand two-cell stages. Development 112, 921-932.
23. Liu, Y., Yan, X. and Zhou, T. (2013). TBCK influences cell proliferation, cell size and mTOR signaling pathway. PLoS ONE 8, e71349.
24. Lois, C., Hong, E. J., Pease, S., Brown, E. J. and Baltimore, D. (2002). Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295, 868-872.
25. Mayer, W., Niveleau, A., Walter, J., Fundele, R. and Haaf, T. (2000). Embryogenesis: demethylation of the zygotic paternal genome. Nature 403, 501-502.
26. Meissner, A., Mikkelsen, T. S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B. E., Nusbaum, C., Jaffe, D. B. et al. (2008). Genomescale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766-770.
27. Mu, W., Munroe, R. J., Barker, A. K. and Schimenti, J. C. (2010). PDCD2 is essential for inner cell mass development and embryonic stem cell maintenance. Dev. Biol. 347, 279-288.
28. Necsulea, A., Soumillon, M., Warnefors, M., Liechti, A., Daish, T., Zeller, U., Baker, J. C., Grützner, F. and Kaessmann, H. (2014). The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 505, 635-640.
29. Oswald, J., Engemann, S., Lane, N., Mayer, W., Olek, A., Fundele, R., Dean, W., Reik, W. and Walter, J. (2000). Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 10, 475-478.
30. Pages, H., Aboyoun, P., Gentleman, R. and DebRoy, S. (2013). Biostrings: String Objects Representing Biological Sequences, and Matching Algorithms. R package version 2. 32 0.
31. Pall, G. S., Wallis, J., Axton, R., Brownstein, D. G., Gautier, P., Buerger, K., Mulford, C., Mullins, J. J. and Forrester, L. M. (2004). A novel transmembrane MSP-containing protein that plays a role in right ventricle development. Genomics 84, 1051-1059.
32. Park, S.-J., Komata, M., Inoue, F., Yamada, K., Nakai, K., Ohsugi, M. and Shirahige, K. (2013). Inferring the choreography of parental genomes during fertilization from ultralarge-scale whole-transcriptome analysis. Genes Dev. 27, 2736-2748.
33. Patel, R. K. and Jain, M. (2012). NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS ONE 7, e30619.
34. Rinn, J. L., Kertesz, M., Wang, J. K., Squazzo, S. L., Xu, X., Brugmann, S. A., Goodnough, L. H., Helms, J. A., Farnham, P. J., Segal, E. et al. (2007). Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129, 1311-1323.
35. Santos, F., Peters, A. H., Otte, A. P., Reik, W. and Dean, W. (2005). Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev. Biol. 280, 225-236.
36. Sigova, A. A., Mullen, A. C., Molinie, B., Gupta, S., Orlando, D. A., Guenther, M. G., Almada, A. E., Lin, C., Sharp, P. A., Giallourakis, C. C. et al. (2013). Divergent transcription of long noncoding RNA/mRNA gene pairs in embryonic stem cells. Proc. Natl. Acad. Sci. USA 110, 2876-2881.
37. Smallwood, S. A., Tomizawa, S.-i., Krueger, F., Ruf, N., Carli, N., Segonds- Pichon, A., Sato, S., Hata, K., Andrews, S. R. and Kelsey, G. (2011). Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat. Genet. 43, 811-814.
38. Smith, Z. D., Chan, M. M., Mikkelsen, T. S., Gu, H., Gnirke, A., Regev, A. and Meissner, A. (2012). A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484, 339-344.
39. Strumpf, D., Mao, C.-A., Yamanaka, Y., Ralston, A., Chawengsaksophak, K., Beck, F. and Rossant, J. (2005). Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132, 2093-2102.
40. Teperek-Tkacz, M., Pasque, V., Gentsch, G. and Ferguson-Smith, A. C. (2011). Epigenetic reprogramming: is deamination key to active DNA demethylation? Reproduction 142, 621-632.
41. Tomikawa, J., Shimokawa, H., Uesaka, M., Yamamoto, N., Mori, Y., Tsukamura, H., Maeda, K.-i. and Imamura, T. (2011). Single-stranded noncoding RNAs mediate local epigenetic alterations at gene promoters in rat cell lines. J. Biol. Chem. 286, 34788-34799.
42. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L. and Pachter, L. (2012). Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578.
43. Tsai, M.-C., Manor, O., Wan, Y., Mosammaparast, N., Wang, J. K., Lan, F., Shi, Y., Segal, E. and Chang, H. Y. (2010). Long noncoding RNA as modular scaffold of histone modification complexes. Science 329, 689-693.
44. Uesaka, M., Nishimura, O., Go, Y., Nakashima, K., Agata, K. and Imamura, T. (2014). Bidirectional promoters are the major source of gene activationassociated non-coding RNAs in mammals. BMC Genomics 15, 35.
45. Wang, L., Zhang, J., Duan, J., Gao, X., Zhu, W., Lu, X., Yang, L., Zhang, J., Li, G., Ci, W. et al. (2014). Programming and inheritance of parental DNA methylomes in mammals. Cell 157, 979-991.
46. Yeh, W.-C., de la Pompa, J. L., McCurrach, M. E., Shu, H.-B., Elia, A. J., Shahinian, A., Ng, M., Wakeham, A., Khoo, W., Mitchell, K. et al. (1998). FADD: essential for embryo development and signaling from some, but not all, inducers of apoptosis. Science 279, 1954-1958.
47. Ying, Q.-L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P. and Smith, A. (2008). The ground state of embryonic stem cell selfrenewal. Nature 453, 519-523.
48. Younglai, E. V., Holt, D., Brown, P., Jurisicova, A. and Casper, R. F. (2001). Sperm swim-up techniques and DNA fragmentation. Hum. Reprod. 16, 1950-1953.
49. Zhou, Z., Hong, E. J., Cohen, S., Zhao, W.-N., Ho, H.-Y. H., Schmidt, L., Chen, W. G., Lin, Y., Savner, E., Griffith, E. C. et al. (2006). Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52, 255-269.